Parametric models for predicting nonstationary spike-spike correlations with local field potentials

Correlations between the spiking of pairs of neurons are often used to study the brain’s representation of sensory or motor variables and neural circuit function and dysfunction. Previous statistical techniques have shown how time-averaged spike-spike correlations can be predicted by the time-averaged relationships between the individual neurons and the local field potential (LFP). However, spiking and LFP are both nonstationary, and spike-spike correlations have nonstationary structure that cannot be accounted for by time-averaged approaches. Here we develop parametric models that predict spike-spike correlations using a small number of LFP-based predictors, and we then apply these models to the problem of tracking changes in spike-spike correlations over time. Parametric models allow for flexibility in the choice of which LFP recording channels and frequency bands to use for prediction, and coefficients directly indicate which LFP features drive correlated spiking. Here we demonstrate our methods in simulation and test the models on experimental data from large-scale multi-electrode recordings in the mouse hippocampus and visual cortex. In single time windows, we find that our parametric models can be as accurate as previous nonparametric approaches, while also being flexible and interpretable. We then demonstrate how parametric models can be applied to describe nonstationary spike-spike correlations measured in sequential time windows. We find that although the patterns of both cortical and hippocampal spike-spike correlations vary over time, these changes are, at least partially, predicted by models that assume a fixed spike-field relationship. This approach may thus help to better understand how the dynamics of spike-spike correlations are related to functional brain states. Since spike-spike correlations are increasingly used as features for decoding external variables from neural activity, these models may also have the potential to improve the accuracy of adaptive decoders and brain machine interfaces.